Harmful neutrophil subsets in patients with ischemic stroke: Association with disease severity

Neurol Neuroimmunol Neuroinflamm. 2019 May 15;6(4):e571. doi: 10.1212/NXI.0000000000000571. eCollection 2019 Jul.

Abstract

Objective: To better understand the functional state of circulating neutrophils in patients with ischemic stroke (IS) for planning future clinical trials.

Methods: We analyzed by flow cytometry activation state of circulating neutrophils and the distribution of neutrophil peripheral subsets in 41 patients with acute IS less than 6 hours before admission and compared them with 22 age-matched healthy controls.

Results: Our results demonstrated continuous basal hyperactivation of circulating neutrophils during acute IS, characterized by lower l-selectin expression and higher CD11b expression at the cell surface, increased ROS production by neutrophils, and greater circulating levels of neutrophil elastase. Neutrophil hyperactivation was associated with deregulation of the equilibrium between apoptotic and necrotic. Patients also had higher percentages than controls of the overactive senescent (CXCR4bright/CD62Ldim) neutrophil subset and increased percentage of neutrophils with a reverse transendothelial migration (CD54highCXCR1low) phenotype. Importantly, neutrophil alterations were associated with the clinical severity of the stroke, evaluated by its NIH Stroke Scale score.

Conclusion: Altogether, our results indicate that during acute IS, the inflammatory properties of circulating neutrophils rise, associated with the expansion of harmful neutrophil subsets. These changes in neutrophil homeostasis, associated with disease severity, may play an instrumental role by contributing to systemic inflammation and to the blood-brain barrier breakdown. Our findings highlight new potential therapeutic approaches of stroke by rebalancing the ratio of senescent to immunosuppressive neutrophils or decreasing reverse neutrophil transmigration or both.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Aging
  • Brain Ischemia
  • CD11b Antigen / metabolism
  • Cell Adhesion Molecules / metabolism
  • Cell Death
  • Cytokines / metabolism
  • Female
  • Healthy Volunteers
  • Humans
  • Immunosuppression Therapy
  • Inflammation
  • L-Selectin / metabolism
  • Leukocyte Elastase / metabolism
  • Longitudinal Studies
  • Male
  • Middle Aged
  • Neutrophil Activation
  • Neutrophils / pathology*
  • Neutrophils / physiology*
  • Prospective Studies
  • Reactive Oxygen Species / metabolism
  • Stroke / blood
  • Stroke / pathology*

Substances

  • CD11b Antigen
  • Cell Adhesion Molecules
  • Cytokines
  • ITGAM protein, human
  • Reactive Oxygen Species
  • SELL protein, human
  • L-Selectin
  • Leukocyte Elastase